Introduction

The stability of a mechanical system may be defined as the time taken to return to its initial state when perturbed by external forces or torques. Thus a stable chair is one which, when tipped so that two legs rise of the ground, returns to its initial upright position with all four legs in contact. A chair that returns to this state immediately may be said to be more stable than one that alternately rocks onto opposing pairs of legs several times before settling on all four legs. Correspondingly, the stability of someone standing upright may be defined as the speed with which the initial quiet standing state is restored after a horizontal push at waist level (Gilles et al., 1999). For example, a 10 N (1 kg) horizontal forward push at the level of the pelvis will accelerate body Centre of Mass (CoM) forward relative to the base of support. Restoration of the initial state involves a postural reflex including toe-down ankle torque generated by the calf plantar flexors (gastrocnemius, soleus). The speed of that response will depend on a number of factors including the level of sensory input, the amplitude of the muscle response, intra- and inter-segmental coordination of muscle activation. Sensory motor disorder, such as hemiparetic stroke with asymmetrically reduced sensory input, slowed, weakened and incoordinated muscle activation, can profoundly affect the standing stability assessed by a horizontal forward push. And such impairment would also be expected to signal that difficulties would arise in practical contexts such as maintaining stable standing on transport systems where the base of support is subject to horizontal accelerations e.g. on a bus or train.

Quiet standing without external perturbations is also a challenge for the Central Nervous System (CNS). The CoM is located somewhat in front of the ankle so that upright posture must be maintained by the ankle muscles. Passive stiffness of the ankle muscles and tendons can prevent around 90% of the tendency to dorsiflexion (Lakie et al., 2003; Loram & Lakie, 2002a; Loram & Lakie, 2002b). However, this is not sufficient to prevent forward sway so active muscle contraction is indicated. Loram and Lakie (Loram & Lakie, 2002a; Loram & Lakie, 2002b) used very small perturbations to the ankle and show no phasic activation of calf muscles. Instead they argued for intermittent anticipatory adjustments of the muscle resting length to vary stiffness and hence change the forward lean (Loram et al., 2005).

In order to perceive both self-motion and motion of a dynamic environment when maintaining body balance, the human CNS has at its disposal multiple sensory channels (Horak & Macpherson, 1996) including vision, vestibular sensation, leg muscle proprioception and tactile sensations in the soles of the feet. Deprivation of any one of these senses or the inability to resolve conflict between sensory cues, potentially caused by disorders of the peripheral or central nervous system, invariably causes conspicuous instability and increases in body sway (Dichgans & Diener, 1989; Diener & Dichgans, 1988). In fact, the detection of body sway by means of somatosensory input channels (muscle proprioception and cutaneous plantar sensation) plays a predominate role during quiet stance (Fitzpatrick & McCloskey, 1994). Body sway in a static posture means that the CoM moves relative to the feet which causes not only stretch in lower limb muscles but also changes the pressure distribution under the feet. Modulating plantar tactile sensation and perceived length of distal leg muscles by local vibratory stimulation directly affects body sway as much as perceived postural orientation and body tilt (Kavounoudias et al., 1998; Kavounoudias et al., 2001; Roll et al., 2002). Therefore, Roll and Roll and colleagues (Kavounoudias et al., 2001) suggested that both modalities are combined additively into one representation of body orientation for sway control.

The versatility of the human postural control system, however, also enables us to utilize other sensory channels, such as non-plantar skin receptors, for the control of body sway. Of course, a prerequisite of this feat is that these afferences convey body sway-related information. For example, upper limb tactile feedback, for example from the fingertips, can be recruited as a sensory source about body sway. In the following review we will present the current state of knowledge concerning mechanisms involved in the processing of tactile afferent information for the optimization of body balance in quiet stance and locomotion. We will begin with a discussion of the traditional approach investigating sway feedback by means of light touch during quiet standing. It follows a summary of light touch effects on sway in the aging population and patients with sensorimotor impairments and increased fall risk. In this context, consideration of object-mediated light contact such as sticks and canes is also relevant. We will then discuss evidence that high-order anticipatory processes are also likely to be involved in sway control when contacting an external reference location. From the static contact situation, we will move on to more dynamic postural situations in which the contact is kept with a reference showing own motion dynamics or where the participant him- or herself is actively involved in locomotion. We will then tackle current knowledge about central integration mechanisms for light touch control of balance. We will conclude our review with an overview of the role of tactile feedback during postural and locomotor development in early infancy.

Basic findings in quiet stance

Strong interactions between multiple sensory modalities occur with respect to the representation of the orientation of our body and its segments, such as the eyes, head or limbs, relative to its environment. Uncertainty about the state of the body or a limb can give rise to sensorimotor illusions. Is additional tactile and proprioceptive information available, however, state estimates can be improved in their accuracy which suppresses any illusory states. For example, when prolonged fixation of a visual target is required involuntary ocular drift is observed that correlates with perceived illusory self-motion (“autokinesis”) (Barlow, 1952). Extra somatosensory information about the location of the fixation target, however, for example by grasping the target’s mount, improves the stability of fixations and reduces the self-motion illusion (Lackner & Zabkar, 1977). Further, illusory arm movement induced by muscle tendon vibration will be suppressed if the other arm touches the stimulated arm after onset of vibration, but not if touch is established before onset (Lackner & Taublieb, 1983). Given the benefit of somatosensory information for spatial limb orientation estimates, one can ask whether this effect generalizes to more complex postural tasks such as upright standing balance, perhaps in terms of improved representation of the gravitational vertical or better localization relative to the environment? Indeed, this seems to be the case.

Lackner, Jeka and colleagues (Holden et al., 1994) showed in healthy participants that mechanically non-supportive fingertip contact (<1 N) with an earth-fixed reference while the eyes are closed results in reductions in sway, which may be even more efficient than vision alone (Jeka & Lackner, 1994; Lackner et al., 1999). Cross-correlation time lags indicated that the force signal at the fingertip precedes postural adjustments, which implies feedback processing of touch for sway control (Jeka & Lackner, 1994). The processing of the touch signal is affected by the relative position of the touch location to the body and the contacting limb posture. Depending on the current body posture and the relative position of the contact, a "radial" touch signal, meaning a touch vector directed parallel to the dominant direction of sway, is more effective than a "laminar" touch vector orthogonal to the sway plane (Jeka et al., 1998b). Nevertheless, the touch effect seems to be independent of the degrees of freedom of the contacting limb in contrast to the precision with which contact is being kept (Rabin et al., 2008).

Skin feedback can also be utilized when the tactile contact is received passively (Krishnamoorthy et al., 2002; Rogers et al., 2001). Cutaneous receptors sensitive to skin stretch detecting differences in shear forces at the contact location but also muscle proprioception of the contacting upper limb provide feedback about the direction and amplitude of body sway relative to the contact location (Rabin et al., 1999). Fingertip contact modulates the H reflex of the soleus muscle (Huang et al., 2009). Simultaneous contact of both hands to reference locations induces greater sway reduction than a single hand contact (Dickstein, 2005), which indicates that sensory summation works in this modality too. Withdrawal of the differential by keeping the relative position of the contact constant to the body (Reginella et al., 1999) or removal of finger tactile feedback by tourniquet ischemia removes the attenuation of body sway with light touch (Kouzaki & Masani, 2008). Finally, it has been shown that the contacting location does not need to be earth-fixed since haptic force feedback from holding a weight via a non-rigid link such as a cable or string reduces body sway as well (Krishnamoorthy et al., 2002; Mauerberg-deCastro et al., 2010; Mauerberg-deCastro et al., 2012).

Compensation for sensorimotor impairments

Baldan et al. (Baldan et al., 2014) reviewed the literature on the effect of light touch on postural sway in individuals with balance problems due to aging, brain lesions or other motor or sensory deficits. The effect of light touch on body sway was found irrespective of the impaired balance. They suggested that the maintenance of the fingertip lightly touching an external reference point could provide somatosensory information for individuals with poor balance universally. In healthy individuals, light touch has been demonstrated to counter the disruptive effects (spatial disorientation by proprioceptive distortion and abnormal motor commands) of neck muscle vibration as well as peroneal muscle tendon and Achilles tendon vibration on body sway (Lackner et al., 2000; Bove et al., 2006; Caudron et al., 2010). Older adults retain the ability to use fingertip contact for augmentation of body sway feedback despite reductions in their tactile sensitivity (Tremblay et al., 2004). In fact, older adults tend to show even greater efficacy of touch feedback for sway reduction than younger adults possibly due to greater sensory loss in distal parts of the lower extremities (Baccini et al., 2007).

Interestingly, blind individuals appear to have an advantage in terms of the tactile integration latency compared to sighted individuals (Schieppati et al., 2014), which implies that in sighted individuals intermodal integration involving both the visual and tactile sensory systems (even when visual feedback is currently not available) makes up a significant portion of processing time. A more detailed discussion of the factors affecting integration of tactile as well as visual information for body balance can be found in a recent review by Honeine and Schieppati (Honeine & Schieppati, 2014).

Object-mediated contact effects

Jeka (Jeka, 1997) suggested that augmented haptic feedback supplied by handles of canes and sticks might lead to the development of mobility aids for balance-impaired populations. A cane as a hand-held tool allows a much greater number of contacting degrees of freedom and therefore variation of haptic force feedback compared to any earth-fixed stand. Indeed, cane-mediated ground contact benefits sway if force feedback is sufficiently strong and correlated to body sway (Albertsen et al., 2010; Albertsen et al., 2012). Jeka and colleagues (Jeka et al., 1996) showed that blind individuals' sway benefits significantly from holding a cane, especially when contacting the ground in a slanted orientation. In addition, Albertsen and colleagues (Albertsen et al., 2012) demonstrated that holding a long stick contacting the ground increases postural stability in young and older adults irrespective of whether the contact location of the stick was earth-fixed or spatially unconstrained due to a low-friction surface over which the contact could slide as a result of participants' body motion. These effects also generalize to an unstable seated posture when holding a pen in younger and older adults (Albertsen et al., 2014).

Light touch as a suprapostural task

When fixating an external visual target at varying distances, postural sway is modulated by the demands of the oculomotor task in terms of minimizing retinal slip of the target (Stoffregen et al., 1999). Thus, looking at the target can be considered a “suprapostural” task to the control of body sway. Similarly, the requirement of lightly keeping contact during standing and walking, for example precise control of the contacting forces in terms of the perceived tactile variability, may represent explicit and implicit goals of a suprapostural task with an external focus of attention (McNevin et al., 2013; McNevin et al., 2000; McNevin & Wulf, 2002; Riley et al., 1999). Riley and co-workers (Riley et al., 1999) demonstrated that the light touch effect on sway is dependent on the salience of the contact within the current postural context. In other words, participants, for whom finger contact occurred only coincidentally, did not show any reductions in sway. That the light touch effect is not only a consequence of tactile feedback processing is also indicated by evidence in favour of proactive sway control. It is remarkable that merely the intention to establish light contact with an earth-fixed reference soon (<5s) can result in effects on body sway similar to actual contact (Bove et al., 2006). Schieppati and colleagues (Bove et al., 2006) proposed that transient anticipatory processes are involved in the preparation of the central postural set to the context of stance control with light contact.

Contact with a reference possessing own motion dynamics

Contact with a non-biological reference location that demonstrates its own oscillatory motion causes involuntary postural sway entrainment as well as increases in body sway compared to a static contact for oscillation frequencies less than 0.8 Hz (Jeka et al., 1998a; Jeka et al., 1997). The default (mis-)attribution of any tactile sensation to own body motion as the origin results in postural adjustments coordinated with the motion of the external source. Thus, body sway oscillations will become synchronized to the velocity as well as the position of the contact point (Jeka et al., 1998a). Interestingly, this effect of spontaneous postural entrainment to a moving contact may be used for closed-loop driving postural sway of an individual (Verite et al., 2014). It is surprising in this respect that contact to a dynamic reference such as another human (light interpersonal touch; IPT) actually reduces postural sway and leads to interpersonal sway synchronization potentially, but not necessarily, due to similar entrainment mechanisms (Johannsen et al., 2009; Johannsen et al., 2012). This reduction of sway during contact with another individual may also be caused by mechanisms involved in the reduction of sway by low-noise vibratory stimulation of the fingertip or the foot soles ("stochastic resonance" resulting in enhanced somatosensory feedback; (Collins et al., 2003; Kimura et al., 2012; Magalhaes & Kohn, 2011; Magalhaes & Kohn, 2012; Priplata et al., 2003)). Passive exposure to the recorded sway dynamics of another individual via a haptic force feedback device, however, does not result in the sway reductions seen during contact with an actual human partner (Wing et al., 2011). This implies that sway reduction with IPT reflects a mutually adaptive process between two contacting individuals. This interaction does not seem to be the result of a mechanical coupling between both individuals but instead represents the effect of mutually shared sensory information (Reynolds & Osler, 2014). The IPT phenomenon has implications for clinical assistance with the balance of neurological patients. For example, sway reduction with passively received IPT has also been reported in patients with chronic stroke and Parkinson's disease as a function of the contact location (Johannsen et al., 2014b).

Effects of interpersonal touch have also been reported during overground walking. Hausdorff and colleagues (Zivotofsky & Hausdorff, 2007; Zivotofsky et al., 2012) reported that when two individuals walk next to each other strong and spontaneous synchronization can be observed, especially when interpersonal tactile feedback is present, for example by holding hands. In this context, tactile and auditory cues appear more effective than visual feedback alone (Zivotofsky et al., 2012) Zivotofsky and Hausdorff (Zivotofsky & Hausdorff, 2007) suggested that this interpersonal entrainment, perhaps enhanced by interpersonal touch, may be used to facilitate the locomotor pattern in individuals with impaired gait.

Central processing for tactile integration

Tactile feedback delays of about 300 ms duration as reported in several studies suggest supraspinal pathways affording complex processing (Clapp & Wing, 1999; Jeka & Lackner, 1994; Rabin & Gordon, 2006). Utilizing light touch for sway control demands attention (Vuillerme et al., 2006). This may be related to high-order processing of the tactile feedback or representation of the postural context. For example, Franzen and colleagues (Franzen et al., 2011) suggested that the postural control system switches between reference frames (from a global to a local trunk-centred) during the integration of light touch. Studies of the time course of sway before, during and after periods of intermittent touch indicate that sway stabilization with light tactile contact is a time-consuming integrative process (Rabin et al., 2006; Sozzi et al., 2012). Initial integration of touch information into the postural control loop seems to happen in a third of the time (100-300 ms) required for the integration of visual information (Lackner & DiZio, 2005; Rabin et al., 2006). In other situations, however, the processing of touch for postural control may be more complex than the processing of visual feedback and therefore may require longer integration latencies due to increased computational load (Sozzi et al., 2012). Nevertheless, sway reduction following integration of fingertip afferent information into the postural control loop occurs between 1.5 to 2 seconds after contact onset (Rabin et al., 2006). Compared to periods of 2 second (or shorter) intermittent fingertip contact, intermittent contact of just 5 second duration results in an after-effect on sway in terms of a reduced return rate to no contact levels (Johannsen et al., 2014a). This after-effect may indicate that the integration of fingertip contact requires no less than about 2 seconds of computation and is likely to involve not only bottom-up sensory processing but also top-down, "intentional" control of body sway and tactile attention.

An indication of the involvement of cortical processes in the light touch effect on sway is the observation that the disruption of the right-hemisphere prefrontal cortex of the brain by continuous theta-burst transcranial magnetic stimulation (cTBS) modulates the processing of somatosensory evoked potentials during standing with contact to an earth-fixed reference location (Bolton et al., 2011; Bolton et al., 2012). In addition, Johannsen et al. (Johannsen et al., 2015) showed that disruption of left inferior parietal gyrus by 1 Hz repetitive TMS (rTMS) alters the time course of sway following unpredictable contact removal. This finding is another indication that top-down tactile attentional processes may have a prominent influence on the control of body sway during postural state transitions.

Developmental aspects

Interpersonal support as well as external earth-fixed balance support plays a prominent role in the early development of motor capabilities such as standing and walking. Lacquaniti and colleagues (Ivanenko et al., 2005) demonstrated in toddlers who had just begun to walk independently how unilateral single hand support with a parent improves postural stability in terms of reduced trunk sway, sideways hip motion as well as step width. Older children, two years and above, did not show any similar effects. Ivanenko et al. (Ivanenko et al., 2005) interpreted these benefits as an indication of increased toddlers' stepping confidence.

On the other hand, there is evidence that early stage toddlers are quite susceptible to tactile input that conveys self-motion information gained from contact with an environmental reference. Metcalfe, Clark and colleagues (Chen et al., 2007; Chen et al., 2008; Metcalfe et al., 2005a; Metcalfe et al., 2005b) conducted a longitudinal study on the development of upright standing and walking in infants and toddlers. They assessed body sway in a quiet posture, sitting on a saddle-styled support and standing, at regular intervals from one month before to nine months after the onset of independent walking. In addition, body sway in the respective posture was assessed with and without static external light touch. When standing, variability of sway did not change a lot across the observation period. The sway dynamics, however, indicated a progression towards a lower sway frequency. The availability of hand light touch reduced the variability and the frequency of sway even further. Metcalfe, Clark and colleagues (Chen et al., 2008; Metcalfe et al., 2005b) interpreted this as an indication for a progressively refined internal representation of own sway dynamics during standing and walking in toddlers. In the semi-sitting posture in contrast to upright standing, hand light touch reduced sway only during the transition period when the toddlers began to take their first independent steps (Chen et al., 2007).

It can easily be imagined that tactile feedback from a contacting hand represents a highly salient sensory signal during the transition to independent walking. When contacting a support, every voluntary step as well as every unintended sway excursion will cause correlated tactile feedback. Thus, it seems reasonable to assume that the tactile feedback resembles an important error signal in the course of learning to walk independently. This notion is confirmed by Barela et al. (Barela et al., 1999), who demonstrated that the utilization of tactile information in the context of postural control changes its qualitative character after the onset of independent walking. Cross-correlation analysis indicated that before this event, body sway had a very short lead of about 45 ms on the contact forces, expressing mechanical support functions of the contact, while afterwards sway was following the contacting forces by about 140 ms. The authors suggested that the tactile contact from that point on facilitates anticipatory postural control in the toddlers (Barela et al., 1999). Metcalfe and Clark (Metcalfe & Clark, 2000) elaborated on this conclusion by suggesting that the tactile signal enhances the exploration of perception-action relationship for the generation of internal models for the control of body balance during standing and walking.

Conclusions

In this chapter we have reviewed how light tactile contact to the fingertips or other body segments improves the control of body balance in quiet stance as well as locomotion. We interpret the effects, which extend to light contact with moving targets, such as another individual, as representing augmented self-motion feedback. The context of keeping light touch, however, imposes task demands which are likely to influence the selection of any concurrent postural strategy. Therefore, keeping light touch requires both proactive as well as reactive balance control. Interpretation of any tactile signal in the current postural context involves high-order representations, which are still understood poorly. Nevertheless, the beneficial effect of tactile information for the control of body balance is quite robust and has been demonstrated in a number of neurological disorders. Thus, the findings reviewed have implications for rehabilitation and handling of neurological patients.

Acknowledgements

We acknowledge the financial support by the Biotechnology and Biological Sciences Research Council of the United Kingdom (BBSRC; BBI0260491) and the Federal Ministry of Education and Research of Germany (BMBF; 01EO1401).

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